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Changes in the status of tortoise populations in Greece 1984–2001
Abstract
Three species of tortoise (Testudinidae) occur in Greece (Testudo hermanni, T. graeca and the endemic T. marginata), all of which have been listed as rare or vulnerable. This paper describes the current situation of 75 populations that were last observed in the 1970s and 1980s and described in 1989. Twenty-nine populations had declined in density and/or status (significantly more than had improved), 10 of which were functionally extinct. A particularly notable loss was a dense population of T. marginata at Gytheion in the Peloponnese due to a widespread fire. Declining populations were significantly associated with identified high threat in 1989 and with close proximity to human settlement. There were no significant effects of tortoise species, area of site, characteristics of surrounding areas or original density on these changes. Declines were less associated with agriculture than predicted in 1989, reflecting changing economic conditions in Greece in the 1990s. Continuing threats to tortoise habitats make their long-term future appear bleak outside of protected areas. The risk of extinction from stochastic variation in small populations was also assessed, using the VORTEX program. This risk was much lower than that from habitat loss; 60–96% of populations of 100 tortoises would survive for 1000 years, depending on adult body size, compared to only 0–0.02% of habitats. The high survival potential of small populations would facilitate conservation of the high intraspecific diversity of tortoises in Greece.
... Our data did not allow for robust population size and density estimations; hence we only calculated the densities of marked individuals in their respective sites. (Miller et al. 2001;Hailey and Willemsen 2003). Instead of testing a wide spectrum of scenarios to account for many possible demographic and conservation scenarios, we used actual field data, and where appropriate, we implemented realistic, sitespecific threats. ...
... Nevertheless, 100 y are likely insufficient to assess population viability in a species where individual longevity can exceed 50 y and generation time is about 20 y (Hailey 1990;Shoemaker et al. 2013;Reed and McCoy 2014). Therefore, to follow the recommendations of Hailey and Willemsen (2003) and Reed and McCoy (2014) on running PVAs for Greek populations of T. h. boettgeri and other chelonians, respectively, we also performed 1,000-y simulations. ...
... PVAs have seldom been applied to tortoise populations (Miller et al. 2001;Hailey and Willemsen 2003). Miller et al. (2001) suggested that isolated populations of the Gopher Tortoise (Gopherus polyphemus) may persist unless substantial perturbations occur, such as an increase in disease prevalence or in juvenile mortality. ...
According to the International Union for Conservation of Nature (IUCN), more than half of all chelonian species are seriously threatened. Habitat loss and illegal trade contribute substantially to this trend. Rare and vulnerable taxa often enjoy formal protection while taxa with large populations are usually neglected, despite worrying trends. The two subspecies of the Hermann's Tortoise (Testudo hermanni) present a good example of this contrast: the western subspecies (T. h. hermanni) is rare, while the eastern conspecific (T. h. boettgeri) is still relatively common in appropriate habitats. The IUCN lists the entire species as Near Threatened. In practice, the western subspecies is treated as endangered, while the assessment of the conservation status of the eastern counterpart is still lacking. Using field data collected from five populations of T. h. boettgeri in three Balkan countries, we aim at filling this gap. Population Viability Analyses (PVAs) suggest that even large and dense populations inhabiting favorable environments could face extinction by over-harvesting in a matter of years. Natural causes (e.g., higher female mortality) or stochastic events (e.g., wildfires) could be detrimental to peculiar isolated populations. The uncertain viability of the studied populations casts considerable doubt over the apparent stability of T. h. boettgeri. For this subspecies to avoid the fate of its western cousin, we propose the upgrade of its IUCN category to Vulnerable throughout its distribution range.
... Testudines are the rarest group of native herpetofauna on these islands and appear to be continually declining. A variety of threats to their habitat make the long-term future of Testudines uncertain outside of protected areas (Hailey and Willemsen 2003). ...
The Sporades are one of the most biologically important archipelagos in the Aegean Sea (Greece) and have received priority conservation over the last 50 years. However, despite numerous early efforts, its herpetofauna is only partially described, resulting in many distributional gaps that have prevented adequate understanding and management of the resident species communities. We review one century of bibliography from the Northern Sporades and combine this information with a review of museum specimens and insights from numerous extensive field surveys over the last near-decade to provide for the first time a comprehensive picture of the reptiles and amphibians of the archipelago. We report here on 26 new island records and find that the herptile communities of the region are largely derived from the herpetofauna of the nearby Thessaly mainland, with only a few introduced taxa. There is also a small but significant set of endemic taxa in the archipelago. Island species richness declines with decreasing island size and increasing duration of island isolation. Herptile communities on smaller islands are progressively nested subsets of the communities on larger islands. The presence of reptile species depends sensitively on the condition and management of native ecosystems. While non-aquatic species maintain largely healthy populations, most populations are under pressure from the combined effects of rampant tourist development, the destruction and degradation of rare wetland habitats, and the abandonment of traditional agricultural landscapes. We provide recommendations regarding sustainable management of the local reptile and amphibian populations.
... Habitat loss and fragmentation are mediated by numerous factors, such as agricultural expansion and intensification, urbanization, tourist infrastructure development and recreational activities, the pet trade and climate change. All these threats are causing a landscape change worldwide (Forman et al. 2003;Bürgi et al. 2004;Jaeger et al. 2007) affecting numerous wildlife species (Grift 1999;Underhill and Angold 2000;Marzluff 2001), as well as the eastern populations of T. hermanni (Willemsen and Hailey 1989;Hailey and Willemsen 2003;Pătroescu and Rozylowicz 2007;Türkozan et al. 2008;Rozylowicz and Dobre 2010;Ljubisavljević et al. 2011Ljubisavljević et al. , 2014Nikolić et al. 2018). Hence, landscape use intensification is globally one of the most significant land-use changes (Ellis et al. 2021) that directly contribute to habitat loss and modification, especially in western European countries (Couturier et al. 2014). ...
Hermann’s tortoise ( Testudo hermanni ) is listed as “Near threatened” in the IUCN Red list of endangered species. The importance of protecting the Hermann’s tortoise populations and its habitats have led to the inclusion of the species within CITES Convention (Annex II), Annex A of EU Wildlife Trade Regulation, Annex II of the Bern Convention and Annexes II and IV of the EU Habitats Directive. To assess the distribution and status of the eastern Hermann’s tortoise ( Testudo hermanni boettgeri ) in Croatia, historical and recent records were gathered and analyzed. The species was recorded in all three biogeographical regions in the country, but it’s native to the Mediterranean and a small part of the Alpine region. With the increase of recent surveys and the use of citizen science platforms, the known range of the species in Croatia was increased by 35.8% and is now encompassing 123 10 × 10 km EEA reference grid cells. Most records (66%) originate from lower elevations (up to 199 m), and the highest was recorded at 570 m. Sparse forests are the most preferred habitats, followed by semi-open habitats, such as grasslands and shrubs. The most serious threat to the species is natural succession due to the increased abandonment of traditional farming and grazing. Other threats include touristic infrastructure and urban development, transportation, illegal collecting, and invasive species. The Area of Occupancy calculated using 2 × 2 km grids resulted in an AOO of 1,372.00 km ² , while Extent of Occurrence (EOO) is calculated to be 18,145.07 km ² . The current network of National protected areas includes 14% of the species’ AOO while the designated Natura 2000 areas include 29.30% of its AOO. We propose to designate an additional 10 Natura 2000 areas to help with the long-term protection of the species.
... Golden eagle breeding metrics can be negatively affected where main prey availability (tortoises in our case) declines or altogether collapses [3,81,82]. Both tortoise species have an unfavourable conservation status and a declining population trend, the Hermann's tortoise populations are considered Vulnerable (VU) [77,83], threatened by excess mortality and habitat loss through agricultural intensification, land abandonment, development and wildfires [84]. Such pressures are widespread in Mediterranean woodlands and garrigue [85] that dominate much of our population's distribution range. ...
Golden Eagles are resident in Greece and known to feed mainly on tortoises when breeding. However, information on alternative prey is scarce, especially during the tortoise brumation, that roughly coincides with the eagles’ non-breeding season. We analyzed 827 prey items collected from 12 territories over five territory years and 84 records of eagles hunting or feeding behavior. Tortoises dominated the breeding season diet (71% of prey categories on average) and over half of all hunting/feeding observations. While no spatial structure was evident, habitat variables such as forest canopy cover were important associates in golden eagle diet seasonally. A significant seasonal pattern emerged in diet diversity, using a subset of six territories with at least 10 samples per season. Eagles shifted from a narrow, reptile- based breeding season diet dominated by tortoises to a broader non-breeding season diet, that included more carrion, mammals and birds. Breeding season specialization on ectothermic prey is a trait usually associated with migratory raptors in the Western Palearctic. The observed dietary diversity expansion accompanied by residency in the absence of ectothermic prey, highlights the adaptability of the golden eagle, a generalist predator. Tortoise populations in Greece are of conservation concern and land use changes as well as climate change, such as development and land abandonment may increase the prevalence of catastrophic megafires, exacerbating the threats to the golden eagle’s main prey when breeding. We discuss this and other diet related conservation implications for the species in northern Greece.
... In general, it is clear that turtles and tortoises are among the most threatened vertebrates on earth (Ihlow et al., 2012;Aulyia et al., 2016;Rhodin et al., 2018;Stanford et al., 2020) also due to their peculiar life-history traits (e.g., Heppel, 1998). However, long-term field studies on population declines of chelonians can be logistically very complicated because of the ecological features of these vertebrates (elusive habits realized with low densities; and are therefore still scarce with in most studies only indirect evidence of their decline (Stubbs & Swingland, 1985;Hailey, 2000;Hailey & Willemsen, 2003;Fernández-Chacón et al., 2011). Thus, the present study represents a contribution in this issue, and suggests that many tortoise populations may actually be in decline also in the temperate regions of Europe, despite it being thought so far that the tropical and subtropical populations were particularly at risk (Rhodin et al., 2018;Stanford et al., 2020). ...
Long-term ecological studies are important for understanding wild populations' dynamics and processes and the actual factors that can determine their decline. Here, we report the results of a 28-years-long (1992-2019) monitoring of three distinct populations of a tortoise, Testudo hermanni, in Central Italy, with an emphasis on their population abundance trends and on the eventual variation in their habitat use across years and among the study areas. Samplings were conducted by Visual Encounter Survey (VES) methodology, and using a suite of statistical analyses including correlations and Generalized Linear Models analyses. Our data showed a statistically significant decline in tortoise sightings through time, and concurrently also a variation in habitat use by tortoises. In all the three study areas, we observed a significant increase of tortoise sighting frequency in the habitat type characterized by high (>taller than 200 cm) shrubby and wooded vegetation. Since our analyses revealed no significant change in the habitat type availability by year in each study area, we suggest that T. hermanni was increasingly selecting closed vegetation spots throughout the years. We hypothesize that this observed trend of shift in habitat selection could be due to lowering their body temperatures to prevent overheating. So, the selection of more covered spots would be a thermal ecology adaptive consequence of the ongoing global warming.
... boettgeri) appears to be better, with more numerous populations [8,9]. However, recent studies have shown that even numerous populations on the Balkan Peninsula might become vulnerable due to rapid changes in demography and/or habitat destruction [3,10]. ...
The Hermann's tortoise (Testudo hermanni) is among the conservation priorities in the
European Union. Consequently, it is included in Annexes II and IV of the EU Habitats Directive, Annex II of the Bern Convention, and Annex II of the CITES Convention. Hermann’s tortoise conservation programs compile insight on the threats affecting population viability, along with factors shaping the species’ distribution. Serbian opulations of the eastern subspecies (Testudo hermanni boettgeri) seem numerous and therefore prosperous, but recent population viability analyses revealed that they are susceptible to rapid demographic changes and/or habitat destruction. This implies the
need for effective population monitoring and protection, as well as mapping and conservation of suitable habitats. In this paper we summarized current knowledge about the geographic distribution of the Hermann's tortoise in Serbia and modeled its ecological niche. Our results corroborate and uphold the known species’ distribution in Serbia. Most suitable habitats are situated in the lowland areas of eastern, central and southern Serbia, at lower altitude slopes under semi-open habitats, such as pastures and shrubs, broad leaf forests, and all successional stages in between. The results provided in this paper should be considered in the selection and shaping of NATURA 2000 sites in Serbia.
... In general, no 'normal' simulations Willemsen (2003)]. We plugged in actual field data (Table 13) and data from literature (Hailey and Loumbourdis 1988;Hailey 1990;Willemsen and Hailey 2003;Bertolero et al. 2011;Couturier et al. 2014) For more details on the methodology please see . ...
Two populations, island and mainland, of promiscuous sexually coercive Hermann tortoises (Testudo hermanni, a species with delayed maturity ~10 years) from the Prespa Region in Macedonia were scrutinized. Prior maturity, tortoises first grow slowly, thereafter gradually increase growth speed, variation in body size and survival probability (mean annual survival rate: 0.30 to 0.70). Potential for indeterminate growth, progressive hardening of the carapace and a survival plateau at the age of five (0.90) promote inter-individual variations in growth trajectories and a wide range of adult asymptotic sizes. Our data question the classical notion of a given size at maturity; instead progressive raise of testosterone levels suggests that maturity is established in growing males ranging from 115 to 140mm in body length. In the Testudo genus females are larger than males; asymptotic estimates of body size show that the studied populations make no exception. Yet, the largest island tortoises are males. With ~100 individuals/ha and an operational sex ratio (OSR ♂/♀) of ~11, male sexual coercion provokes cloacal injuries to females and reduces their body-condition, increasing female mating costs. Male adult survival (0.97) is greater compared to female survival (0.84). Island females do not live long, are discouraged from reproduction and low recruitment further exacerbates OSR-bias, eventually leading to population extinction. Where females suffer and are underrepresented, frustrated males exhibit frequent same-sex sexual behaviours along with extravagant sexual behaviours. The results are discussed in a conservation framework.
... Actually, none of the seven species (four terrapins and three tortoises) is identified as present in arable lands. We ran a literature search to retrieve data on the presence of these species on arable lands, which provided records solely referring to terrestrial tortoises (Testudo sp.), indicating that the progression of agriculture is causing fragmentation and extinction of populations (Hailey and Willemsen 2003, Anadón et al. 2007, Perez et al. 2012, Couturier et al. 2014). However, the presence of tortoises, and in particular of Hermann's tortoise (Testudo hermanni) in areas of traditional agriculture not exposed to intense mechanisation has been reported (Bertolero et al. 2011), which could make this species a suitable chelonian model. ...
... boettgeri són en una millor situació de conservació. Cal remarcar, però, que es disposa de menys informació sobre l'estat real de les poblacions d'aquesta última subespècie i que moltes d'elles també estan patint processos de rarificació en temps recents (Hailey i Willemsen, 2003;Rocylowics i Dobre, 2010). En l'àmbit d'espècie, i per a tot el seu rang de distribució, es proposa que la tortuga mediterrània sigui catalogada com a Quasi Amenaçada a la llista vermella de la IUCN (Bertolero et al., en premsa). ...
Chelonian trouble: threats and future Challenge for its Conservation. – Among the 324 spe-
cies of chelonians currently known, approximately one-quarter are currently threatened with extinc-
tion. The factors leading to the disappearance of these species have been directly linked to human
activity. Major threats include the increasing commercial trade that drives the overexploitation of
many species, the lucrative market for products derived from turtles (traditional Chinese medicine
and decorative objects), both legal and illegal pet markets, and habitat loss. In this context, some
species are now very scarce, having only a few dozen individuals in surviving populations, while
there is even a species with only one living individual still in existence. In the case of the Hermann’s
tortoise, while some of its populations (e.g., in l’Albera, Alt Empordà) or in certain regions (Roma-
nia) survive at critically low levels, its overall situation is not as severe and therefore it is currently
classed as “almost threatened” by the IUCN. The general causes of its disappearance are some-
what similar to those affecting most of the chelonian species. Nevertheless, Hermann’s tortoise
is not currently eaten and its main threats stem from the loss of habitat, poaching, and significant
increases in the populations of its predators. If the most threatened populations are to recover, it
is necessary to implement efficient management of their habitat and to eliminate poaching, which
affects both natural and reintroduced populations. In terms of the latter, we need to teach people
to see the Hermann’s tortoise as a wild animal, so they will be able to understand that its place is
the wild.
Two species of endangered tortoises occur in Spain: the Spur-thighed tortoise (Testudo graeca) and Hermann's tortoise. The are three separate populations of the Spur-thighed tortoise: one in southwestern Spain (Parque Nacional de Doñana), another in the southeast (provinces of Murcia and Almeria) and a third one in northwestern Mallorca. Hermann's tortoise inhabits the north eastern corner of the country, the southern part of Mallorca and most of Minorca.
Population Viability Analysis (PVA) is the estimation of extinction probabilities by analyses that incorporate identifiable threats to population survival into models of the extinction process. Extrinsic forces, such as habitat loss, over-harvesting, and competition or predation by introduced species, often lead to population decline. Although the traditional methods of wildlife ecology can reveal such deterministic trends, random fluctuations that increase as populations become smaller can lead to extinction even of populations that have, on average, positive population growth when below carrying capacity. Computer simulation modelling provides a tool for exploring the viability of populations subjected to many complex, interacting deterministic and random processes. One such simulation model, VORTEX, has been used extensively by the Captive Breeding Specialist Group (Species Survival Commission, IUCN), by wildlife agencies, and by university classes. The algorithms, structure, assumptions and applications of VORTEX are described in this paper. VORTEX models population processes as discrete, sequential events, with probabilistic outcomes. VORTEX simulates birth and death processes and the transmission of genes through the generations by generating random numbers to determine whether each animal lives or dies, to determine the number of progeny produced by each female each year, and to determine which of the two alleles at a genetic locus are transmitted from each parent to each offspring. Fecundity is assumed to be independent of age after an animal reaches reproductive age. Mortality rates are specified for each pre-reproductive age-sex class and for reproductive-age animals. Inbreeding depression is modelled as a decrease in viability in inbred animals. The user has the option of modelling density dependence in reproductive rates. As a simple model of density dependence in survival, a carrying capacity is imposed by a probabilistic truncation of each age class if the population size exceeds the specified carrying capacity. VORTEX can model linear trends in the carrying capacity. VORTEX models environmental variation by sampling birth rates, death rates, and the carrying capacity from binomial or normal distributions. Catastrophes are modelled as sporadic random events that reduce survival and reproduction for one year. VORTEX also allows the user to supplement or harvest the population, and multiple subpopulations can be tracked, with user-specified migration among the units. VORTEX outputs summary statistics on population growth rates, the probability of population extinction, the time to extinction, and the mean size and genetic variation in extant populations. VORTEX necessarily makes many assumptions. The model it incorporates is most applicable to species with low fecundity and long lifespans, such as mammals, birds and reptiles. It integrates the interacting effects of many of the deterministic and stochastic processes that have an impact on the viability of small populations, providing opportunity for more complete analysis than is possible by other techniques. PVA by simulation modelling is an important tool for identifying populations at risk of extinction, determining the urgency of action, and evaluating options for management.
The structure of the VORTEX computer simulation model for population viability analysis is outlined. The program flow is described here in order to provide a detailed specification of the structure of a widely used population viability analysis model. VORTEX is an individual-based simulation program that models the effects of mean demographic rates, demographic stochasticity, environmental variation in demographic rates, catastrophes, inbreeding depression, harvest and supplementation, and metapopulation structure on the viability of wildlife populations. The model facilitates analysis of density-dependent reproduction and changing habitat availability, and most demographic rates can optionally be specified as flexible functions of density, time, population gene diversity, inbreeding, age, and sex. VORTEX projects changes in population size, age and sex structure, and genetic variation, as well as estimating probabilities and times to extinction and recolonization.
Energetic aspects of female reproduction are described for Testudo graeca, T. marginata and T. hermanni (3 populations of different body size) from N Greece. Clutch size, clutch mass and annual egg repoduction varied with body size between populations. Mean relative clutch mass ranged from 4-7%, and was highest in T. hermanni. All populations laid 2-3 clutches per year. Annual reproductive effort as a proportion of body content was c15% in all populations, lower than in other reptiles, partly because the carapace accounts for over half of the total ash-free dry weight of the tortoise body. -from Authors
The area of dark pigmentation on the plastron of the tortoise Testudo hermanni shows a latitudinal cline over about 400 km in Greece, with populations in the south being darker. The carapace did not show the clinal trend, and pigmentation was not significantly related to longitude or altitude. We examined several possible explanations for the cline, including an effect of incubation temperature, random genetic variation, and adaptation to several environmental variables. The most likely explanation is selection for thermoregulation, with decreased dark pigmentation in the north reducing heat loss to the substrate by infra red radiation during activity. This hypothesis was supported by data on body (T(b)) and substrate (T(s)) temperatures in populations from northern, central and southern Greece. T(b) was generally above T(s), showing that heat would generally be lost rather than gained through the plastron, and the mean difference T(b)-T(s) was greatest in the north: +6.6 °C, compared to +2.4 °C in the south. Mean T(b) was lowest in the south (26.9°C, compared to 29.3°C in the north) and the slope of T(b) on T(s) was about 1 (compared to 0.5 in the north). Thermoregulation in southern Greece is similar to that of tropical tortoises, with avoidance of overheating being the major problem, rather than elevation of T(b) for activity.
The impact of fire and mechanical habitat destruction on a population of the tortoise Testudo hermanni in northern Greece varied with vegetation type and season. A major fire in summer 1980 caused low (10 cm) in coastal heath, highest (about 50%) mortality in grassland, and intermediate levels in dry heath. Mechanical habitat destruction caused about 50% mortality in affected areas. Mortality of juveniles was greater than that of sexable animals. Overall, the 1980 catastrophe was more damaging than previously thought, causing a 64% decrease in the total size of the Alyki main heath population. A localized summer fire in 1986 caused a similar level and pattern of mortality to that of 1980, but a spring fire in 1988 had little effect on the tortoise population. A fire and mechanical habitat destruction in winter 1989/90 caused only a 14% decrease in population size; mortality was again concentrated in grassland areas, but affected juveniles and sexable animals equally. Variation of mortality with season suggests that any burning needed for habitat management at tortoise sites should occur in winter or early spring. Juveniles were undersampled by 3–4 times compared to sexable animals; their number increased greatly by 1990, reaching the same proportion as in the original population. There was, however, no recovery in the number of sexable tortoises in the decade after the 1980 catastrophe.